What has proteomics taught us about Leishmania development?

Parasitology

Volumn 139, Issue 9, 2012, Pages 1146-1157

  Tsigankov, Polina ^a   Gherardini, Pier Federico ^b   Helmer Citterich, Manuela ^b   Zilberstein, Dan ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

differentiation; intracellular parasitism; Leishmania; proteomics

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ACYL CARRIER PROTEIN; ARGININE; ASPARAGINE; ASPARTIC ACID; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUCOSE 6 PHOSPHATE ISOMERASE; GLUTAMIC ACID; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HISTIDINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; INITIATION FACTOR 2ALPHA; IRON SUPEROXIDE DISMUTASE; ISOCITRATE DEHYDROGENASE; MALATE DEHYDROGENASE; MESSENGER RNA; METHIONINE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE 7; OXIDOREDUCTASE; PROTEIN TYROSINE KINASE; RNA; SQUALENE MONOOXYGENASE; SUCCINATE DEHYDROGENASE; SUPEROXIDE DISMUTASE; TRIOSEPHOSPHATE ISOMERASE; TRYPANOTHIONE; TRYPANOTHIONE REDUCTASE;

AMASTIGOTE; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL STRUCTURE; DOWN REGULATION; ENERGY METABOLISM; FATTY ACID OXIDATION; FATTY ACID SYNTHESIS; GENE EXPRESSION; GLUCONEOGENESIS; IN VITRO STUDY; IN VIVO STUDY; LEISHMANIA; LEISHMANIA DONOVANI; LEISHMANIA MEXICANA; MITOCHONDRIAL MEMBRANE; NONHUMAN; OXIDATIVE STRESS; PARASITE DEVELOPMENT; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEOMICS; SIGNAL TRANSDUCTION; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INSECT VECTORS; LEISHMANIA; LEISHMANIASIS; LIFE CYCLE STAGES; MACROPHAGES; PHAGOSOMES; PROTEOMICS; PROTOZOAN PROTEINS; PSYCHODIDAE; SIGNAL TRANSDUCTION;

EID: 84864999160     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182012000157     Document Type: Article

References (81)

1. Alcolea, P. J., Alonso, A., Gomez, M. J., Sanchez-Gorostiaga, A., Moreno-Paz, M., Gonzalez-Pastor, E., Torano, A., Parro, V. and Larraga, V. (2010). Temperature increase prevails over acidification in gene expression modulation of amastigote differentiation in Leishmania infantum. BMC Genomics 11, 31. doi: 10.1186/1471-2164-11-31.
2. Antoine, J. C., Prina, E., Jouanna, C. and Bongrand, P. (1990). Parasitophorous vacuoles of Leishmania amazonensis - infected macrophages maintain an acidic pH. Infecion and Immunity 58, 779-787.
3. Aslet, T. M., Aurrecoechea, C., Berriman, M., Brestelli, J., Brunk, B. P., Carrington, M., Depledge, D. P., Fischer, S., Gajria, B., Gao, X., Gardner, M. J., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Hertz-Fowler, C., Houston, R., Innamorato, F., Iodice, J., Kissinger, J. C., Kraemer, E., Li, W., Logan, F. J., Miller, J. A., Mitra, S., Myler, P. J., Nayak, V., Pennington, C., Phan, I., Pinney, D. F., Ramasamy, G., Rogers, M. B., Roos, D. S., Ross, C., Sivam, D., Smith, D. F., Srinivasamoorthy, G., Stoeckert, C. J., Jr., Subramanian, S., Thibodeau, R., Tivey, A., Treatman, C., Velarde, G. and Wang, H. (2010). TriTrypDB: A functional genomic resource for the Trypanosomatidae. Nucleic Acids Research 38, D457-462. doi: 10.1093/nar/gkp851.
4. Barak, E., Amin-Spector, S., Gerliak, E., Goyard, S., Holland, N. and Zilberstein, D. (2005). Differentiation of Leishmania donovani in host-free system: Analysis of signal perception and response. Molecular and Biochemical Parasitology 141, 99-108.
5. Bates, P. A. (1994). The developmental biology of Leishmania promastigotes. Experimental Parasitology 79, 215-218.
6. Bates, P. A., Robertson, C. D., Tetley, L. and Coombs, G. H. (1992). Axenic cultivation and characterization of Leishmania mexicana amastigoteslike forms. Parasitology 105, 193-202.
7. Bengs, F., Scholz, A., Kuhn, D., and Wiese, M. (2005). LmxMPK9, a mitogen-activated protein kinase homologu affects flagellar length in Leishmania mexicana. Molecular Microbiology 55, 1606-1615. doi: 10.1111/j.1365-2958.2005. 04498.x
8. Berman, J. D., Goad, L. J., Beach, D. H. and Holz, G. G., Jr. (1986). Effects of ketoconazole on sterol biosynthesis by Leishmania mexicana mexicana amastigotes in murine macrophage tumor cells. Molecular and Biochemical Parasitology 20, 85-92.
9. Berman, J. D., Holz, G. G., Jr. and Beach, D. H. (1984). Effects of ketoconazole on growth and sterol biosynthesis of Leishmania mexicana promastigotes in culture. Molecular and Biochemical Parasitology 12, 1-13.
10. Blum, J. J. (1993). Intermediary metabolism of Leishmania. Parasitology Today 9, 118-122.
11. Blum, J. J. (1994). Energy metabolism in Leishmania. Journal of Bioenergetics and Biomembranes 26, 147-155.
12. Burchmore, R. J. and Barrett, M. P. (2001). Life in vacuoles. International Journal for Parasitology 31, 1311-1320.
13. Cammerer, S. B., Jimenez, C., Jones, S., Gros, L., Lorente, S. O., Rodrigues, C., Rodrigues, J. C., Caldera, A., Ruiz Perez, L. M., da Souza, W., Kaiser, M., Brun, R., Urbina, J. A., Gonzalez Pacanowska, D. and Gilbert, I. H. (2007). Quinuclidine derivatives as potential antiparasitics. Antimicrobial Agents and Chemotherapy 51, 4049-4061. doi: 10.1128/AAC.00205-07.
14. Chow, C., Cloutier, S., Dumas, C., Chou, M. N. and Papadopoulou, B. (2011). Promastigote to amastigote differentiation of Leishmania is markedly delayed in the absence of PERK eIF2alpha kinase-dependent eIF2alpha phosphorylation. Cell Microbiology 13, 1059-1077. doi: 10.1111/j.1462-5822.2011. 01602.x
15. Debrabant, A., Joshi, M. B., Pimenta, P. F. and Dwyer, D. M. (2004). Generation of Leishmania donovani axenic amastigotes: Their growth and biological characteristics. International Journal for Parasitology 34, 205-217.
16. Erdmann, M., Scholz, A., Melzer, I. M., Schmetz, C. and Wiese, M. (2006). Interacting protein kinases involved in the regulation of flagellar length. Molecular Biology of the Cell 17, 2035-2045.
17. Fernandes, A. B., Neira, I., Ferreira, A. T. and Mortara, R. A. (2006). Cell invasion by Trypanosoma cruzi amastigotes of distinct infectivities: Studies on signaling pathways. Parasitology Research 100, 59-68.
18. Field, M. C. (2005). Signalling the genome: The Ras-like small GTPase family of trypanosomatids. Trends in Parasitology 21, 447-450. doi:10.1016/j.pt.2005.08.008.
19. Field, M. C. and O,Reilly, A. J. (2008). How complex is GTPase signaling in trypanosomes? Trends in Parasitology 24, 253-257.
20. Forestier, C. L., Machu, C., Loussert, C., Pescher, P. and Spath, G. F. (2011). Imaging host cell-Leishmania interaction dynamics implicates parasite motility, lysosome recruitment, and host cell wounding in the infection process. Cell Host and Microbe 9, 319-330.
21. Ginger, M. L., Chance, M. L. and Goad, L. J. (1999). Elucidation of carbon sources used for the biosynthesis of fatty acids and sterols in the trypanosomatid Leishmania mexicana. Biochemical Journal 342, 397-405.
22. Glaser, T. A., Baatz, J. E., Kreishman, G. P. and Mukkada, A. J. (1988). pH homeostasis in Leishmania donovani amastigotes and promastigotes. Proceeding of the National Academy of Sciences, USA 85, 7602-7606.
23. Glaser, T. A., Utz, G. L. and Mukkada, A. J. (1992). The plasma membrane electrical gradient (membrane potential) in Leishmania donovani promastigotes and amastigotes. Molecular and Biochemical Parasitology 51, 9-15.
24. Gosline, S. J., Nascimento, M., McCall, L. I., Zilberstein, D., Thomas, D. Y., Matlashewski, G. and Hallett, M. (2011). Intracellular eukaryotic parasites have a distinct unfolded protein response. Plos ONE 6, e19118. doi:10.1371/journal.pone.0019118.
25. Hart, D. T. and Coombs, G. H. (1982). Leishmania mexicana: Energy metabolism of amastigotes and promastigotes. Experimental Parasitology 54, 397-409.
26. Hem, S., Gherardini, P. F., Osorio y Fortea, J., Hourdel, V., Morales, M. A., Watanabe, R., Pescher, P., Kuzyk, M. A., Smith, D., Borchers, C. H., Zilberstein, D., Helmer-Citterich, M., Namane, A. and Spath, G. F. (2010). Identification of Leishmania-specific protein phosphorylation sites by LC-ESI-MS/MS and comparative genomics analyses. Proteomics 10, 3868-3883. doi: 10.1002/pmic.201000305.
27. Holm, A., Tejle, K., Gunnarsson, T., Magnusson, K. E., Descoteaux, A. and Rasmusson, B. (2003). Role of protein kinase C alpha for uptake of unopsonized prey and phagosomal maturation in macrophages. Biochemical and Biophysical Research Communication 302, 653-658.
28. John Von Freyend, S., Rosenqvist, H., Fink, A., Melzer, I. M., Clos, J., Jensen, O.N. and Wiese, M. (2010). LmxMPK4, an essential mitogen-activated protein kinase of Leishmania mexicana is phosphorylated and activated by the STE7-like protein kinase LmxMKK5. International Journal for Parasitology 40, 969-978. doi:10.1016/j.ijpara.2010.02.004.
29. Kimblin, N., Peters, N., Debrabant, A., Secundino, N., Egen, J., Lawyer, P., Fay, M. P., Kamhawi, S. and Sacks, D. (2008). Quantification of the infectious dose of Leishmania major transmitted to the skin by single sand flies. Proceeding of the National Academy of Sciences, USA 105, 10125-10130.
30. Lahav, T., Sivam, D., Volpin, H., Ronen, M., Tsigankov, P., Green, A., Holland, N., Kuzyk, M., Borchers, C., Zilberstein, D. and Myler, P. J. (2011). Multiple levels of gene regulation mediate differentiation of the intracellular pathogen Leishmania. FASEB Journal 25, 515-525. doi: 10.1096/fj.10-157529.
31. Laxman, S. and Beavo, J. A. (2007). Cyclic nucleotide signaling mechanisms in trypanosomes: Possible targets for therapeutic agents. Molecular Interventions 7, 203-215.
32. Lorente, S. O., Rodrigues, J. C., Jimenez Jimenez, C., Joyce-Menekse, M., Rodrigues, C., Croft, S. L., Yardley, V., De Luca-Fradley, K., Ruiz-Perez, L. M., Urbina, J., De Souza, W., Gonzalez Pacanowska, D. and Gilbert, I. H. (2004). Novel azasterols as potential agents for treatment of leishmaniasis and trypanosomiasis. Antimicrobial Agents and Chemotherapy 48, 2937-2950.
33. Lukacs, G. L., Rotstein, O. R. and Grinstein, S. (1991). Determinants of the phagosomal pH in macrophages. In situ assessment of vacuolar H+-ATPase activity, counterion conductance, and H+ "Leak". Journal of Cell Biology 266, 24540-24548.
34. Maere, S., Heymans, K. and Kuiper, M. (2005). BiNGO: A Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21, 3448-3449.
35. Mazareb, S., Fu, Z. Y. and Zilberstein, D. (1999). Developmental regulation of proline transport in Leishmania donovani. Experimental Parasitology 91, 341-348.
36. McNeely, T. B., and Turco, S. J. (1990). Requirement of lipophosphoglycan for intracellular survival of Leishmania donovani within human monocytes. Journal of Immunology 144, 2745-2750.
37. Moraes, M. C., Jesus, T. C., Hashimoto, N. N., Dey, M., Schwartz, K. J., Alves, V. S., Avila, C. C., Bangs, J. D., Dever, T. E., Schenkman, S. and Castilho, B. A. (2007). Novel membrane-bound eIF2alpha kinase in the flagellar pocket of Trypanosoma brucei. Eukaryotic Cell 6, 1979-1991.
38. Morales, M. A., Renaud, O., Faigle,W., Shorte, S. L. and Spath, G. F. (2007). Over-expression of Leishmania major MAP kinases reveals stagespecific induction of phosphotransferase activity. International Journal for Parasitology 37, 1187-1199.
39. Morales, M. A., Watanabe, R., Laurent, C., Lenormand, P., Rousselle, J. C., Namane, A. and Spath, G. F. (2008). Phosphoproteomic analysis of Leishmania donovani pro- and amastigote stages. Proteomics 8, 350-363. doi: 10.1002/pmic.200700697.
40. Mottram, J. C. and Coombs, G. H. (1985). Leishmania mexicana: Enzyme activities of amastigotes and promastigotes and their inhibition by antimonials and arsenicals. Experimental Parasitology 59, 151-160.
41. Mukkada, A. J., Meade, J. C., Glaser, T. A. and Bonventre, P. F. (1985). Enhanced metabolism of Leishmania donovani amastigotes at acid pH: An adaptation for intracellular growth. Science 229, 1099-1101.
42. Mukkada, A. J., Schaefer, F.W., III., Simon, M.W. and Neu, C. (1974). Delayed in vitro utilization of glucose by Leishmania tropica promastigotes. Journal of Protozoology 21, 393-397.
43. Muller, I. B., Domenicali-Pfister, D., Roditi, I. and Vassella, E. (2002). Stage-specific requirement of a mitogen-activated protein kinase by Trypanosoma brucei. Molecular Biology of the Cell 13, 3787-3799.
44. Naderer, T., Dandash, O. and McConville, M. J. (2011). Calcineurin is required for Leishmania major stress response pathways and for virulence in the mammalian host. Molecular Microbiology 80, 471-480.
45. Naderer, T., Ellis, M. A., Sernee, M. F., De Souza, D. P., Curtis, J., Handman, E. and McConville, M. J. (2006). Virulence of Leishmania major in macrophages and mice requires the gluconeogenic enzyme fructose-1,6- bisphosphatase. Proceeding of the National Academy of Sciences, USA 103, 5502-5507.
46. Naderer, T., Heng, J. and McConville, M. J. (2010). Evidence that intracellular stages of Leishmania major utilize amino sugars as a major carbon source. Plos Pathogens 6, e1001245.
47. Opperdoes, F. R. and Coombs, G. H. (2007). Metabolism of Leishmania: Proven and predicted. Trends in Parasitology 23, 149-158.
48. Paape, D., Barrios-Llerena, M. E., Le Bihan, T., Mackay, L. and Aebischer, T. (2010). Gel free analysis of the proteome of intracellular Leishmania mexicana. Molecular and Biochemical Parasitology 169, 108-114.
49. Paape, D., Lippuner, C., Schmid, M., Ackermann, R., Barrios-Llerena, M. E., Zimny-Arndt, U., Brinkmann, V., Arndt, B., Pleissner, K. P., Jungblut, P. R. and Aebischer, T. (2008). Transgenic, fluorescent Leishmania mexicana allow direct analysis of the proteome of intracellular amastigotes. Molecular and Cellular Proteomics 7, 1688-1701.
50. Parsons, M., Worthey, E. A., Ward, P. N. and Mottram, J. C. (2005). Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. BMC Genomics 6, 127. doi:10.1186/1471-2164-6-127.
51. Pescher, P., Blisnick, T., Bastin, P. and Spath, G. F. (2011). Quantitative proteome profiling informs on phenotypic traits that adapt Leishmania donovani for axenic and intracellular proliferation. Cell Microbiology 13, 978-991. doi:10.1111/j.1462-5822.2011.01593.x
52. Rivas, L. and Chang, K. P. (1983). Intraparasitophorous Vacuolar pH of Leishmania mexicana Infected Macrophages. Biological Bulletin 165, 536-537.
53. Rodrigues, J. C., Bernardes, C. F., Visbal, G., Urbina, J. A., Vercesi, A. E. and De Souza, W. (2007). Sterol methenyl transferase inhibitors alter the ultrastructure and function of the Leishmania amazonensis mitochondrion leading to potent growth inhibition. Protist 158, 447-456.
54. Rosenzweig, D., Smith, D., Myler, P. J., Olafson, R.W. and Zilberstein, D. (2008a). Post-translational modification of cellular proteins during Leishmania donovani differentiation. Proteomics 8, 1843-1850.
55. Rosenzweig, D., Smith, D., Opperdoes, F., Stern, S., Olafson, R.W. and Zilberstein, D. (2008b). Retooling Leishmania metabolism: From sand fly gut to human macrophage. FASEB Journal 22, 590-602.
56. Saar, Y., Ransford, A., Waldman, E., Mazareb, S., Amin-Spector, S., Plumblee, J., Turco, S. J. and Zilberstein, D. (1998). Characterization of developmentally-regulated activities in axenic amastigotes of Leishmania donovani. Molecular and Biochemical Parasitology 95, 9-20.
57. Sacks, D. L. (1989). Metacyclogenesis in Leishmania promastigotes. Experimental Parasitology 69, 100-103.
58. Sacks, D. L. and Perkins, P. V. (1985). Development of infective stage Leishmania promastigotes within phlebotomine sand flies. American Journal of Tropical Medicine and Hygiene 34, 456-459.
59. Saunders, E. C.,de Sauza, D. P., Naderer, T., Sernee, M. F., Ralton, J. E., Doyle, M. A., Macrae, J. I., Chambers, J. L., Heng, J., Nahid, A., Likic, V. A. and McConville, M. J. (2010). Central carbon metabolism of Leishmania parasites. Parasitology 137, 1303-1313. doi: 10.1017/S0031182010000077.
60. Saxena, A., Lahav, T., Holland, N., Aggarwal, G., Anupama, A., Huang, Y., Volpin, H., Myler, P. J. and Zilberstein, D. (2007). Analysis of the Leishmania donovani transcriptome reveals an ordered progression of transient and permanent changes in gene expression during differentiation. Molecular and Biochemical Parasitology 152, 53-65.
61. Schroder, M. and Kaufman, R. J. (2005). The mammalian unfolded protein response. Annual Review of Biochemistry 74, 739-789.
62. Stuart, K. D., Schnaufer, A., Ernst, N. L. and Panigrahi, A. K. (2005). Complex management: RNA editing in trypanosomes. Trends in Biochemical Sciences 30, 97-105.
63. Swanson, M. S. and Fernandez-Moreira, E. (2002). A microbial strategy to multiply in macrophages: The pregnant pause. Traffic 3, 170-177.
64. Tovar, J., Wilkinson, S., Mottram, J. C. and Fairlamb, A. H. (1998). Evidence that trypanothione reductase is an essential enzyme in Leishmania by targeted replacement of the tryA gene locus. Molecular Microbiology 29, 653-660.
65. Turco, S. J. (1988). The lipophosphoglycan of Leishmania. Parasitology Today 4, 255-257.
66. Urbina, J. A. (1997). Lipid biosynthesis pathways as chemotherapeutic targets in kinetoplastid parasites. Parasitology 114, 91-99.
67. Vince, J. E., Tull, D., Landfear, S. and McConville, M. J. (2011). Lysosomal degradation of Leishmania hexose and inositol transporters is regulated in a stage-, nutrient- and ubiquitin-dependent manner. International Journal for Parasitology 41, 791-800. doi:10.1016/j. ijpara.2011.02.003.
68. Vinet, A. F., Jananji, S., Turco, S. J., Fukuda, M. and Descoteaux, A. (2011). Exclusion of synaptotagmin V at the phagocytic cup by Leishmania donovani lipophosphoglycan results in decreased promastigote internalization. Microbiology 157, 2619-2628.
69. Wang, Q., Melzer, I. M., Kruse, M., Sander-Juelch, C. and Wiese, M. (2005). LmxMPK4, a mitogen-activated protein (MAP) kinase homologue essential for promastigotes and amastigotes of Leishmania mexicana. Kinetoplastid Biology and Disease 4, 6.
70. Waskiewicz, A. J. and Cooper, J. A. (1995). Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. Current Opinion in Cell Biology 7, 798-805.
71. Wiese, M. (1998). Amitogen-activated protein (MAP) kinase homologue of Leishmania mexicana is essential for parasite survival in the infected host. EMBO Journal 17, 2619-2628.
72. Wiese, M. (2007). LeishmaniaMAPkinases-familiar proteins in an unusual context. International Journal for Parasitology 37, 1053-1062.
73. Wiese, M., Kuhn, D. and Grunfelder, C. G. (2003a). Protein kinase involved in flagellar-length control. Eukaryotic Cell 2, 769-777.
74. Wiese, M., Wang, Q. and Gorcke, I. (2003b). Identification of mitogenactivated protein kinase homologues from Leishmania mexicana. International Journal for Parasitology 33, 1577-1587.
75. Wyllie, S., Cunningham, M. L. and Fairlamb, A. H. (2004). Dual action of antimonial drugs on thiol redox metabolism in the human pathogen Leishmania donovani. Journal of Biological Chemistry 279, 39925-39932.
76. Zhan, K., Vattem, K. M., Bauer, B. N., Dever, T. E., Chen, J. J. and Wek, R. C. (2002). Phosphorylation of eukaryotic initiation factor 2 by heme-regulated inhibitor kinase-related protein kinases in Schizosaccharomyces pombe is important for resistance to environmental stresses 21. Molecular and Cellular Biology 22, 7134-7146.
77. Zilberstein, D. (2008). Physiological and biochemical aspects of Leishmania develpment. In Leishmania After the Genome: Biology and Control, (eds. Myler, P. J. and Fasel, N.), pp. 107-122. New York: Horizon Scientific Press and Caiser Academic Press
78. Zilberstein, D., Agmon, V., Schuldiner, S. and Padan, E. (1984). Escherichia coli intracellular pH, membrane potential, and cell growth. Journal of Bacteriology 158, 246-252.
79. Zilberstein, D., Blumenfeld, N., Liveanu, V., Gepstein, A. and Jaffe, C. L. (1991). Growth at acidic pH induces an amastigote stagespecific protein in Leishmania promastigotes. Molecular and Biochemical Parasitology 45, 175-178.
80. Zilberstein, D., Philosoph, H. and Gepstein, A. (1989). Maintenance of cytoplasmic pH and proton motive force in promastigotes of Leishmania donovani. Molecular and Biochemical Parasitology 36, 109-118.
81. Zilberstein, D. and Shapira, M. (1994). The role of pH and temperature in the development of Leishmania parasites. Annual Review of Microbiology 48, 449-470.